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Phytoprotection

Invasion of the Carribean by the , hirsutus Green [Homoptera : Pseudococcidae] L.A. Sagarra et D.D. Peterkin

Volume 80, numéro 2, 1999 Résumé de l'article Since its accidental introduction into the island of Grenada in 1994, URI : https://id.erudit.org/iderudit/706185ar Maconellicoccus hirsutus [Homoptera : Pseudococcidae], commonly named the DOI : https://doi.org/10.7202/706185ar Hibiscus or Pink Mealybug (HMB), has been inexorably spreading through the islands where it has become a major pest on several crops in 24 Aller au sommaire du numéro Caribbean Islands. This pest was also reported in Guyana threatening South and Central America. M. hirsutus is a very prolific pest that injects a toxin at the point of feeding, causing severe distortion of leaves, new shoots and fruit. Éditeur(s) Initial use of physical and chemical control methods were ineffective. In addition, because of its wide host range and its rapid geographie expansion, Société de protection des plantes du Québec (SPPQ)l not only to agricultural land but also to home gardens and forest areas, biological control appeared as the most suitable method to manage the HMB ISSN populations. Three natural enemies were selected for this biocontrol effort: the predatory beetles Cryptolaemus montrouzieri Mulsant and Scymnuscoccivora 0031-9511 (imprimé) Ramkrisna [Coleoptera : Coccinellidae] and the parasitoid Anagyruskamali 1710-1603 (numérique) Moursi [Hymenoptera : Encyrtidae]. A. kamali and C. montrouzieri were highly effective in bringing HMB populations under control. In newly infested Découvrir la revue countries, early introduction of biological control agents resulted in effective management of the pest. This experience provided a model for future management of other alien invasive pest species in the region. Citer cet article Sagarra, L. & Peterkin, D. (1999). Invasion of the Carribean by the hibiscus mealybug, Maconellicoccus hirsutus Green [Homoptera : Pseudococcidae]. Phytoprotection, 80(2), 103–113. https://doi.org/10.7202/706185ar

La société de protection des plantes du Québec, 1999 Ce document est protégé par la loi sur le droit d’auteur. L’utilisation des services d’Érudit (y compris la reproduction) est assujettie à sa politique d’utilisation que vous pouvez consulter en ligne. https://apropos.erudit.org/fr/usagers/politique-dutilisation/

Cet article est diffusé et préservé par Érudit. Érudit est un consortium interuniversitaire sans but lucratif composé de l’Université de Montréal, l’Université Laval et l’Université du Québec à Montréal. Il a pour mission la promotion et la valorisation de la recherche. https://www.erudit.org/fr/ Symposium / Symposium - Saint-Jean-sur-Richelieu (Québec), Canada 9 juin / 9 June 1999 Ravageurs nouveaux et en ré-émergence / New and re-emerging pests

Invasion of the Caribbean by the hibiscus mealybug, Maconellicoccus hirsutus Green [Homoptera : Pseudococcidae]

L.A. Sagarra1 and D.D. Peterkirr 1 P-R Trinidad Ltd., Orange Grove Estate, Tacarigua, Trinidad & Tobago - W.I.; e-mail: [email protected] 2 CABI Bioscience, Gordon Street, Curepe, Trinidad & Tobago w.i. PHYTOPROTECTION 80: 103-113

ABSTRACT kamali Moursi [Hymenoptera : En- cyrtidae]. A. kamali and C. montrouzieri were highly effective in bringing HMB Since its accidentai introduction into the populations under control. In newly island of Grenada in 1994, Maconelli­ infested countries, early introduction of coccus hirsutus [Homoptera : Pseudo­ biological control agents resulted in coccidae], commonly named the Hibis­ effective management of the pest. This cus or Pink Mealybug (HMB), has been expérience provided a model for future inexorably spreading through the Car­ management of other alien invasive pest ibbean islands where it has become a species in the région. major pest on several crops in 24 Car­ ibbean Islands. This pest was also re- ported in Guyana threatening South and INVASIVE PESTS IN THE Central America. M. hirsutus is a very prolific pest that injects a toxin at the CARIBBEAN point of feeding, causing severe distor- The threat posed by introduced pests tion of leaves, new shoots and fruit. (, plant diseases and weeds) Initial use of physical and chemical reaches far beyond traditional agricul­ control methods were ineffective. In tural production. The advent of an inva­ addition, because of its wide host range sive species into a new environment and its rapid géographie expansion, not may impact on économie activities and only to agricultural land but also to trade. It may also hâve far reaching home gardens and forest areas, biolog- ecological conséquences in terms of ical control appeared as the most suit- altérations to biodiversity and the func- able method to manage the HMB pop­ tion of natural communities of organ­ ulations. Three natural enemies were isais. selected for this biocontrol effort : the predatory beetles Cryptolaemus mon- In a new environment, exotic inva­ trouzieriN\u\sant and Scymnuscoccivo- sive species are usually free from the ra Ramkrisna [Coleoptera : Coccinel- burden of pre-adapted predators, para­ lidae] and the parasitoid Anagyrus sites, pathogens and competitors that

Note du rédacteur ; le texte ci-dessus est présenté tel que soumis/Editor's note : the above text is presented as submitted.

103 kept them in check in their native hab­ INTRODUCTION AND itat. They multiply and spread explo- SPREAD OF M. HIRSUTUS sively, rapidly colonizing and dominat- ing the new environment. This is IN THE CARIBBEAN particularly true in the Caribbean, where each island ecosystem has a spécifie Maconellicoccus hirsutus Green [Ho- flora and fauna which are unusually moptera : Pseudococcidae], commonly susceptible to damage by invasive spe- named the Hibiscus or Pink Mealybug cies. Introduction of exotic species is a (HMB), was first described in by threat to the indigenous species which Green (1908) as Phenacoccus hirsutus could be displaced or even eradicated and was subsequently placed in the due to compétition with the new spe­ genus Maconellicoccusby Ezzat in 1958. cies (Van Driesche and Bellows 1993). It originated from South East (Wil­ This could affect the entire balance of liams 1996) and prior to 1994, it was an ecosystem since the development of widely distributed in numerous coun- the new species is virtually uncontrolled tries of the inter-tropical areas of , and geographical barrier may prevent Asia and (I.I.E. 1997). M. hir­ the natural introduction of pre-adapted sutus was first recorded in the Western competitors from its area of origin. This hémisphère in November 1994, from was the case when the mongoose was the island of Grenada in the Caribbean introduced into the Caribbean to con- (Matille-Ferrero and Etienne 1996), trol snake populations in commercial where it was possibly introduced sev­ crop plantations. In this new environ­ eral years earlier. The origin of the pest ment, mongoose populations increased introduction is still unknown. to such extent that they are now threat- ening certain local snake species which M. hirsutus rapidly spread through were previously controlling populations the Caribbean, increasing its geograph­ of rodents in the islands. ical range from one island in 1994 to four islands in 1995, 7 islands in 1996, Over the last décade, the Caribbean 17 islands in 1997, 20 islands in 1998 has been invaded by several species of and 21 islands in 1999 (Pollard 1998; exotic pests. Thèse include the Etienne, personal communication). melon thrips, Thrips palmi, and the The pest is now présent in Grenada, seed weevil, Sternochetus Trinidad, St. Kitts and Nevis, Saint mangiferea, from Asia, and the brown Maarten, Saint Lucia, Tobago, St. Eusta- aphid, Toxoptera citricida, which tius, Curaçao and possibly Aruba, An- is the most important vector of the cit­ guilla, Guyana, British Virgin Islands, rus tristeza virus, from South Africa via St. Vincent and the Grenadines, US South America. More récent invasions Virgin Islands, Viequez and Culebra Is­ are represented by species like the cit­ lands of Puerto Rico, Monserrat, Guade­ rus leaf miner, Phyllocnistis citrella, loupe, Puerto Rico mainland, and most originally from Asia and Africa, and the recently Martinique was reported to be citrus black fly, Aleurocanthus woglu- infested. To date, the only uninfested mi, from South America. islands of the Lesser Antilles are Barba- Two important mealybug species dos, Dominica and Antigua and Barbu- were also accidentally introduced into da, but the probability of thèse remain- the région within the last 5 years, and ing uninfested is slim. moved rapidly through the islands: Maconellicoccus hirsutus, the hibiscus M. hirsutus generally entered unin­ mealybug from Asia, and Paracoccus fested areas through the ports on con- marginatus from South America (Mat- taminated produce or hidden in pas- ille-Ferrero and Etienne 1998). senger luggage. It rapidly spread along the main routes of human traffic. This This paperwillfocusonthe impact of pattern was repeated in most of the M. hirsutus as a récent invasive pest in infested countries. The hibiscus mealy­ the Caribbean. bug was also spread by wind, animais,

104 SAGARRA, PETERKIN : MACONELLICOCCUS HIRSUTUS IN THE CARIBBEAN

rainfall, human activities and vehicles. long waxy caudal filaments at the pos- In Guyana, the mealybug first spread terior end of the abdomen. The adult within the urban areas and then along females are wingless, dark pink and the rivers which are used as main routes sparsely covered with white waxy fila- for human traffic. mentous sécrétion (Mani 1986). After the completion of egg laying, the fe­ male mealybug shrinks considerably BIOLOGY OF M. HIRSUTUS and ultimately dies. Mani (1986) and Hall (1921) reported both sexual and Like many phytophagous homoptera, parthenogenetic reproduction. M. hirsutus is a sucking insect. Each female deposits between 84 to 654 eggs during 4 to 8 days. The eggs hatch in 3- HOST PLANTS AND 9 days and a génération is usually com­ plétée! within a month (23-35 days) (Ta­ DAMAGE OF M. HIRSUTUS ble 1). Eggs are laid in a loose cottony terminal ovisac, and are orange to pink Maconeilicoccus hirsutus is an extreme- (Ghose 1972). Newly hatched mealy- ly polyphagous species. It affects a total bugs (crawlers) are very mobile, they of 200 plants species around the world settle on the host and start developing. (Berg 1996). In Egypt, severe mealybug This stage is inconspicuous and is re- infestations were observed on Hibiscus sponsible for the rapid spread of the spp. (including cotton), mulberry and pest from initial sites of infestation. Albizzia lebbek. In ail thèse species, Females hâve three and maies hâve four terminal shoots were destroyed giving nymphal instars (Mani 1988). Adult the plants a gnarled appearance (Mani maies hâve one pair of wings, and two 1989). In India, it is a severe pest on

Table 1. Summary of biological data on Maconeilicoccus hirsutus (Sagarra 1999) Particulars Misra Hall Dutt ef al. Singh and Ghose Mani Reddy (1919) (1921) (1951) Ghosh (1972) (1986) and (1970) Narayana (1986) Egg size (Length -mm) 0.36-0.39 - 0.29-0.32 - 0.36-0.40 0.34-0.38 - (Width -mm) 0.15-0.21 - 0.17 0.18-0.21 0.17-0.20 Incubation 5-8 6-9 7 6-7 3-8 4-7 3-4 (days)4 Nymph - - 22 10-19 19-22 20-25 (days) Eggs to adult 24-29 35 - - 23-29 24-27 30 (days) Adult length 2.52 3 - - 2.65-2.80 - (mm) Preoviposition - - 3-5 0.5-6 4-5 - (days) Oviposition - - 5-8 4-5 - 6-8 - (days) Fecundity 232 150-300 194 84-654 386-540 500 (No. of eggs/ female)

105 fiber crops like jute, mesta, roselle, etc. characteristic symptoms: leaf curling, and also on grapevine. Infestation of fruit malformation, bunchy top appear- the growing point resulted in malfor­ ance, etc., due to modification of the mation of shoots and leaves (Mani growth including the shortening of in- 1988). In Saudi Arabia, the hibiscus ternodes. The degree of the symptoms mealybug was found infesting Date dépends on the sensitivity of the crop. Palm fruits, living in large masses on Heavy infestation may cause a com­ the middle stands of the fruit bunches plète défoliation of the plant, leading to (Talhouk 1993). M. hirsutus also affects their death (Dufour and Léon 1997). The a wide range of other crops of économ­ production of honeydew by the pest ie importance including citrus, cocoa, can also cause development of sooty , légumes, grapes, etc. (Berg mould. 1996). It is worth noting that in its area of POTENTIAL ECONOMIC origin the host range is restricted to relatively few plant species (Mani 1989) LOSSES OF M. HIRSUTUS whereas in the Caribbean, over 150 IN THE CARIBBEAN species of tree crops, vegetables, root crops, ornamentals, forest trees and The économie and ecological consé­ weeds are affected by M. hirsutus (Ta­ quences of mealybug infestation ble 2). The most commonly affected through the Lesser Antilles could hâve plants are members of the family Mal- been disastrous. The HMB could spread vaceae including ornamental hibiscus, to ail of the Caribbean Islands and also and . A number of orchard South America. Export of fresh fruits crops such as Citrus spp. and and flowers from the infested area hâve spp. hâve also been affected. Many large been restricted, threatening régional economically important species of tree trade in agricultural products. Hotels such as Blue Mahoe {Hibiscus elatus), hâve experienced increased cost for Samaan (), (Tec- landscaping and replacement of the tona grandis) and Gliricidia spp. hâve infested hibiscus and other ornamental shown extrême susceptibility to this plants. Finally, the timber industry and pest, and many Blue Mahoe and Sa­ watersheds are also under the threat of maan trees hâve died from high infes­ the pink mealybug since the pest af­ tation. Hosts may be divided into two fects several important species of for- catégories, i.e., 1) those on which the est trees. In 1997, USDA estimated that pest can complète its development (e.g. économie losses exceeded US $3.5 mil­ hibiscus, okra, sorrel, samaan, etc.) and lion a year in Grenada and US $125 2) those on which M. hirsutus can feed million a year in Trinidad and Tobago and produce damage symptoms but before control measures were imple- does not complète development (e.g., mented (USDA 1997). green peper, tomatoes, egg plant, etc.). An économie study conducted by L. The hibiscus form colo- Joe Moffit from the University of Mas- o, nies with a very low mobility (Dufour sachussets (1999-unpublished data) §j and Léon 1997). The insect is gregari- showed that the économie risk to Unit­ ZL ous in habit. Both adults and larval ed States agriculture in the event of — instars move to the soft succulent parts invasion of Hibiscus Mealybug is esti­ oo of the plants, infesting tender shoots, mated to be approximately US $750 g buds, pétioles and leaf lamina. During million per year in the absence of con­ p high infestation, they can even remain trol measures. The agricultural crops in y onthe main stem of young plants (Singh the mainland United States expected to £ and Ghosh 1970). As a resuit of its bear most of the économie risk include oc feeding action, the mealybugs inject ornamental crops, vegetable crops, cit­ O toxic saliva into the plant, provoking rus crops, grapes and avocados. > i û.

106 SAGARRA, PETERKIN : MACONELLICOCCUS HIRSUTUS IN THE CARIBBEAN

Table 2. List of plants on which the hibiscus mealybug has been recorded in Trinidad (after Me Comie 1998) Family / scientific name Family / scientific name Family / scientific name Acanthaceae Caricaceae Leguminosae Eranthemum nervosum Carica papaya Acacia spp. Pachystachys lutea Cajanus cajan Casuarinaceae Thunbergia erecta Calliandra spp. Cas u a ri n a spp. Caesalpinia pulcherrima Amaranthaceae Rhoeo spp. Cassia siamea Amaranthus spp. Compositae Cassia fistula Achyranthes indica Bidens pilosa Mimosa pudica Celosia cristata Emilia spp. Samanea saman Anacardiaceae Gergera spp. Tamarindus indica Mangifera indica Parthenium Vigna unguiculata Spondias purpurea hysterophorus Liliaceae Spondias cytherea Syndrella nodiflora densiflorus Annonaceae Convolvulaceae Asparagus setaceus Annona muricata Ipomoea spp. Cordyline terminalis Annona squamosa Dracaena spp. Crassulaceae Canangium odorata Kalanchoe pinnata Lythraceae Annona reticulata Kalanchoe spp. Punica grantum Apocynaceae Lagerstroemia indica Cucurbitaceae Al la manda cathartica Cucurbita moschata Malpighiaceae Catharanthus rose us Malpighia punicifolia Vinca minor Cyperaceae Ervatamia coronaria Cyperus spp. Malvaceae Nerium oleander Abelmoschus esculentus Davalliaceae Hibiscus rosa-sinensis Araceae Nephrolepis biserrata Hibiscus sabdariffa Aglaonema spp. furcans Sida spp. Colocasia esculenta Nephrolepis exaltata Dieffenbachia spp. Moraceae Dioscoreaceae Philodendron spp. Artocarpus communis Dioscorea spp. Scindapsus aureus Artocarpus altilis Syngonium Euphorbiaceae Ficus benjamina podophyllum Acalypha hispada Musaceae Xanthosoma Codiaeum spp. Musa sapientum sagittifolium Euphorbia pulcherrima Euphorbia prostata Myrtaceae Araliaceae Manihot esculenta Callistemon spp. Brassia (Schefflera) Phyllanthus a ma rus Eugenia malaccensis actinophylla Psidium guajava Dizygotheca Gesneriaceae elegantissima Chrysothemis pulchella Nyctaginaceae Bougainvillea spp. Schefflera spp. Heliconiaceae Bigonînaceae Heliconia spp. Oleaceae Bégonia spp. Jasminum spp. Labiatae Crescentia cujete Leonotis nepetifolia Oxalidaceae Tabebua spp. Averrhoa carambola Cordia spp. Lauraceae Persea americanis Palmae Cactaceae Cocos nu ci fera Pereskia bleo=grandifolia

107 Table 2. List of plants on which the hibiscus mealybug has been recorded in Trinidad (after Me Comie 1998) (Continuée!)

Family / scientific name Family / scientific name Family / scientific name Passifloraceae Rubiaceae Umbelliferae Passiflora edulis Ixora spp. Eryngium foetidum Hamelia spp. Pîcrodendraceae Urticacaeae Mussaenda spp. Picrodendron baccatum Laportea aestuans Rutaceae Piperaceae Verbenaceae Aegle marmelos Piper tuberculatum Lantana camara Citrus spp. Piperonia pellucida Stachytarpheta Murraya paniculata jamaicensis Polygonaceae Murraya koenigii Stachytarpheta spp. Coccoloba uvifera Sapindaceae Vitaceae Portulacaceae Blighia sapida Cissus verticillata Portulaca oleraceae Meliococca bijuga Vitis vinifera Portulaca pilosa Scrophulariaceae Grevillea robusta Zingiberaceae Scoparia dulcis Alpi nia spp. Rhamnaceae Solanaceae Ziziphus mauritiana Capsicum frutescens Rosaceae Datura spp. Rosa spp. Solanum melongena Solanum bicolor

CONTROL METHODS OF consciousness on the part of the public M. HIRSUTUS IN THE and to consequently decrease illégal trading and contraband by exporters, CARIBBEAN importers and passengers.

To counteract the Hibiscus Mealybug The impact of thèse measures was infestation into the Caribbean, three limited since 20 additional islands were control stratégies were subsequently infested between 1996 and 1998, and to implemented: date, only four islands of the Lesser Antilles remain uninfested. Plant quarantine measures and awareness campaign in non Physical and chemical control infested countries When M. hirsutuswas first identified in Following the introduction of the mea­ the Caribbean, it was initially thought lybug from Grenada to Trinidad, quar­ that the pest could be eradicated. Erad- antine Systems were strengthened and ication efforts focused on the use of upgraded in ail the neighbouring coun­ pesticides combined with cultural meth- tries to prevent or delay the introduc­ ods, mainly burning of crop residue. In tion of the pest. Législation was enact- Grenada, 90 ha of Blue Mahoe were ed in several countries, for example, in felled in an effort to contain the spread Trinidad and Tobago, M. hirsutus was of the pest. However, it was realized proclaimed to be a "Notifiable Pest" in that while pesticides gave a quick knock- October 1995. This wasfollowed by the down, rapid reinfestations by M. hirsu­ revision of the plant protection régula­ tus occurred necessitating spray cycles tions and the increased surveillance at every 2 to 3 weeks. A number of Chem­ ports of entry. Régional plant protec­ icals and mixtures hâve been used over tion officers were trained in Trinidad to the years in attempts to control HMB identify mealybug species. A régional infestations. Chemical control of the pest public awareness campaign for the West has proved to be difficult since mealy- Indies was conducted to increase the bugs tend to inhabit less accessible

108 SAGARRA, PETERKIN : MACONELLICOCCUS HIRSUTUS IN THE CARIBBEAN

areas such as cracks and crevices of Previous biological control bark, inside fruit bunches and growing programmes points. The mealybugs are also cov- Similar programs to control M. hirsutus ered with a waterproof secreted waxy infestation hâve already been conduct- coating, and its eggs are laid into an ed in Egypt and India. ovisac made up of a knotted mass of long waxy filaments preventing the In Egypt, two coccinellids species and pénétration of water-based sprays. several hymenopterous parasitoids Another problem was the wide host were released in attemptsto control M. range and large size of infested hosts. hirsutus in the 1930s. The lady beetle, It is almost impossible to hâve a spray- Cryptolaemus montrouzieri was import- ing programme that can bear the cost ed from Australia and reared in insec- and cope with the practicalities of treat- taries for periodic releases in Egypt. ing the whole range of infested plants Although the predator eventually be- in an affected area. came established, it did not perform well because there was very poor sur- Cutting and burning of heavily infest­ vival overthe Egyptian winter. Another ed material were also recommended to coccinellid, Scymnus conformais, was follow the pesticide application, but introduced from Indonesia (Java) but reluctance to the continuous use of this species did not establish. Several pesticides led households to concen- parasitoids were introduced from Indo­ trate on the cutting and burning of nesia (Java) throughout the 1930s and shrubs and trees. of thèse Leptomastix phenacocci has The pest continued to spread despite been reported as becoming established. the chemical and physical control mea- However, M. hirsutus control has been sures, the wide scale use of pesticides attributed to the release of Anagyrus for the control of M. hirsutus was grad- kamali, with figures of parasitisation ually phased out with the systematic from field samples ranging from 66- release of biological control agent in 98% (Kamal 1951). In many areas, it the environment. was reported that the mealybug was almost eradicated. Biological control Another success has been achieved AN organisms hâve natural enemies and with the release of the coccinellid pred- hence are potential targets for biolog­ ators in India in the 1970s. Cryptolae­ ical control. This is particularly true for mus montrouzieri was released at a invasive pest species like M. hirsutus number of vineyards in southern India which arrived in the Caribbean without and was reported as achieving effective its spécifie natural enemies and was control of HMB (Mani 1989). C. mon­ able to multiply virtually unchecked. trouzieri has often been used for the Following the limited success of phys­ biological control of mealybugs, and is ical and chemical measures to control usually effective at high pest densities. the pest populations, régional biologi­ Other coccinellid species, Scymnus cal control programs for M. hirsutus coccivora Ramkrishna Ayyar and Scym­ were initiated in 1996. This should en- nus gratioususW\ese, which survive at sure a long-term suppression and con­ lower population levels of the mealy­ trol of this pest, and also reduce consid- bug and hâve lower température thresh- erably costs associated with chemical olds, hâve also been recommended for control. release in addition to C. montrouzieri. Two Anagyrus species, Anagyrus dac- The exotic nature of the mealybug, tylopii and Anagyrus kamali, hâve also and the known effective natural enemy been reported as being key natural complex from its probable area of ori- enemies of the mealybug, achieving par­ gin, indicated that classical biological asitisation rates of 60-70% in the field in control would be the most appropriate late season (Mani 1989). long-term strategy. In such a program, an exotic natural enemy (or enemies) is Finally, in Hawaii, after initial heavy introduced into the récipient country infestations were noted on cultivated usually from the pest's area of origin. hibiscus and Erythrina spp. population

109 numbers dropped, in the présence of Nevis, St. Martin, Guyana, St. Lucia, US parasitoids, to low levels that damage and British Virgin Islands, Guadeloupe, was no longer noted. The parasitoids Curaçao, St. Vincent and the Grena­ were fortuitously introduced with the dines, and Montserrat. The numbers of pest and lately identified as A. kamali natural enemies released in the différ­ (Beardsley 1985). ent countries are presented in Table 3. Caribbean biological control In addition, St. Kitts and Nevis, Puer­ program to Rico (including Viequez and Culebra) In view of the above, several Caribbean and the US Virgin Islands hâve also countries hâve implemented biological released a population of A. kamalifrom control programmes against the Hibis­ Hawaii and Gyranusoidea indica from cus Mealybug. Thèse hâve been joint Egypt provided by USDA (Meyerdirk, efforts involving National Programmes Personal communication). In Puerto with assistance from régional and in­ Rico, only parasitoids were released to ternational organizations like FAO, control the mealybug. CARDI, CABI Bioscience, MCA, the USDA The predatory beetle, C. montrouz- and INRA. ieri, was imported from India and/or the Initially, when the mealybug was only USA and hâve been introduced into ail présent in Grenada, a FAO TCP pro­ of the infested countries. C. montrouz- gram was launched to provide Grenada /"er/has also been released in Barbados with the parasitoid wasp, A. kamali, although the Hibiscus Mealybug is not produced in the UK by CABI Bioscience. yet présent in the country. Mass-pro­ Following the pest spreading through duction was first conducted but it ap- the Caribbean, the parasitoid A. kamali peared to be less cost efficient than was imported from China and locally direct imports of beetles from the USA. mass-produced in Trinidad for releases Another predatory coccinellid, Scym- in the région. This mass-production nus coccivora was also imported from programme of A. kamali was part of the India and released into Grenada, Trin­ technical coopération projectfunded by idad and Tobago, St. Kitts and Nevis, FAO, the actual rearing being conduct- and Montserrat. However, Scymnus ed at CABI Bioscience in Trinidad. The coccivora appeared to hâve little im­ parasitoid was introduced into Grena­ pact on suppressing HMB. da, Trinidad and Tobago, St. Kitts and

Table 3. Natural enemies releases in the Caribbean Country Number of natural enemies releases C. montrouzieri S. coccivora A. kamali G. indica British Virgin Islands 18 000 - 9 500 - Curaçao - - 2 000 - Grenada 2 000 1 925 25 000 1 500 Guyana 56 000 - 15 240 - Montserrat 500 500 9 250 - St. Kitts and Nevis 206 300 1 300 66 000 32 000 St. Lucia 406 000 - 44 525 - St. Vincent 85 416 - 25 330 - Trinidad and Tobago 30 000 9 000 43 670 - Source: country reports presented at the FAO Evaluation workshop on the biological control of the pink hibiscus mealybug, Maconellicoccus hirsutus, in the Caribbean, Trinidad, March 1999.

110 SAGARRA, PETERKIN : MACONELLICOCCUS HIRSUTUS IN THE CARIBBEAN

IMPACT OF THE Saccharococcus sacchari (Cockerell), BIOLOGICAL CONTROL Puto barberi (Cockerell), Nipaecoccus nipae (Newstead), Plotococcus neotro- PROGRAM IN THE picus Williams & Granara de Willink and CARIBBEAN M. hirsutus. Out of nine species of mealybugs présent in the région, A. Initial results from Grenada, Trinidad kamali could only develop successfully and Tobago, St. Kitts and Nevis and St. from M. hirsutus (Sagarra 1999). Such Lucia indicated that A. kamali and C. specificity of the introduced natural montrouzieri hâve become established enemy should hâve minimal consé­ and hâve dispersed from their initial quences on non-target species. release sites and are effectively control- ling populations of M. hirsutus. There is little information on the impact of S. CONCLUSION coccivora. At présent, mealybug popu­ lations are reported as generally low in thèse islands, with the mealybug occur- During the early phase of M. hirsutus ring in significant numbers on approx- infestation in the Caribbean, in the imately 15 plant species. absence of exotic natural enemies from the pest's area of origin, the mealybug The gênerai strategy has been the had attacked numerous host plants, introduction of C. montrouzieri when causing extensive damage to a wide pest populations were high, followed range of agricultural, forestry and orna- by releases of A. kamalito maintain the mental crops. Since then, the régional pest at a low population. Such an ap- programmes were implemented for proach has been suggested for control biological control of HMB. Although 11 of other mealybug species (Greathead new countries were infested by the pest 1977; Panis 1981). since then, tremendous damage, as Recently, there has been much con- observed in Grenada, Trinidad or St. troversy on the indiscriminate introduc­ Kitts and Nevis during the initial stage tion of natural enemies for classical of infestation by HMB, was not subse- biological control since such introduc­ quently observed. This could be ex- tion could disrupt existing natural ene- plained by the early introduction of my complexes of indigenous pests. This natural enemies, principally A. kamali is particularly relevant where the inher- and C. montrouzieri, once the pest was ently fragile ecosystem of small island detected in a new country and its iden- developing states are concerned. Such tity confirmed. In the présence of its introduction should be supported by natural enemies, M. hirsutus rarely sound ecological studies on the biology caused significant damage. Its host and host sélection of the exotic natural range was considerably reduced, as enemies. The extent to which species remaining populations could only be introduced for biological control attacks found on a few preferred host species non-target species and the ecological of Malvaceae, Annonaceae and Legu- conséquences of such attacks are mat- minaceae. To sustain their biological ters of serious concern. Careful assess- control effort, several Caribbean coun­ ment of biocontrol agents and effective tries are developing mass-rearing facil- means of hosttesting is necessary prior ities for natural enemies of HMB to to their introduction to ensure that non- continue producing A. kamali after the target effects are minimized. termination of the régional program. Host species sélection tests were The sociological impact of HMB in­ conducted for the parasitoid A. kamali festation has also been tremendous as in choice and non-choice situation us- awareness campaigns were conducted ing nine major species of Caribbean in ail the Lesser Antilles Islands to in- mealybug. Thèse included Planococcus form the population about this prob- citri (Risso), Planococcus halli Ezzat & lem. People hâve been educated con- McConnel, Dysmicoccusbrevipes (Cock- cerning biological control and now erell), Pseudococcus elisae Borchsenius, understand that spraying their infested

111 hibiscus plants will not eradicate mea- Dutt, N., P.K. Mukerjee, and N. Sen Gupta. lybugs and that they hâve to let the 1951. Preliminary observations on the in­ natural enemies "do their job". In Trin- cidence of Phenacoccus hirsutus Green idad, téléphone hotlines were installée! and its effect on the growth of Hibiscus sabdariffa L and V. altissima Hort. Indi- for the public to obtain free information an J. Agric. Sci. 21 : 231-237. and natural enemies from the Ministry Ezzat, Y.M. 1958. Maconellicoccus hirsutus of Agriculture. At the régional level, the Green, a new genus with redescription of HMB program is the first régional bio- the species (Homoptera : Pseudococ­ logical control program, and its suc- cidae- Coccoidea). Bull. Soc. Entomol. cess may open the doors for further Egypt 42 : 377-388. coopérative projects in that domain. Ghose, S.K. 1972. Biology of the mealybug Several new pests species are spread- Maconellicoccus hirsutus (Green) ing through the région (Paracoccus (Pseudococcidae : ). Indian Agric. 16 : 323-332. marginatus Williams and Granara de Greathead, D.J. 1977. Biological control of Willink, Aleurocanthus woglumi the mealybug (Homoptera : Pseudococcidae) citrus black fly, and Phyllocnistis citrel- with spécial référence to the cassava /athe citrus leaf miner) and some of the mealybug (Phenacoccus manihoti Mat.- expériences gained during the pro­ Ferr.). Pages 70-80 in K.F. Nwanze and K. gramme for régional biological control Leuschner (eds.), Proceedings of the In­ of HMB may be directly applied to find- ternational Workshop on the cassava ing solutions to problems caused by mealybug, Phenacoccus manihoti Mat.- thèse and future invasive pests. Nation­ Ferr. (Pseudococcidae). INERA-M'vuazi, Bas Zaïre, Zaïre. 26-29 June 1997. al, régional, and international efforts to Green, E.E. 1908. Remarks on Indian Scale curtail the invasions are fundamental Insects (Coccidae), part III. With a cata­ to decrease the impact of exotic species logue of ail species hitherto recorded from on human society and the environment. the Indian continent. Mem. Dep. Agric. Indian Ent. Ser. 2 : 15-46. Hall, W.J. 1921. The Hibiscus Mealybug, ACKNOWLEDGEMENT Pseudococcus hibisci(Herr\\p.). Bull. Soc. Entomol. Egypt 14 : 17-29. I.I.E. (International Institute of Entomology) We thank C. Vincent, Horticulture Re­ 1997. Distribution map of pest, séries A search and Development Research Cen- (Agricultural) map #100 (2nd revision) Ma­ ter, Agriculture and Agri-Food Canada, conellicoccus hirsutus. Saint-Jean-sur-Richelieu, Québec, Can­ Kamal, M. 1951. Biological control projects ada, for commenting an early version in Egypt, with a list of introduced para­ of the manuscript. sites and predators. Bull. Soc. Fouad 1er Entomol. 35 : 205-220. Mani, M. 1986. Distribution, bioecology and management of the grape mealybug REFERENCES Maconellicoccus hirsutus (Green) with a spécial référence to its enemies. Ph.D. Beardsley, J.W. 1985. Pseudococcidae. /nC.P. thesis, UAS, Bangalore. Clausen (éd.), Introduced Parasites and Mani, M. 1988. Bioecology and management Predators of Pests and Weeds, of grapevine mealybug. Ind. Inst. Hortic. a world review. U.S. Dept. Agric. Hand- Res. - Tech. Bull. No. 31 pp. book 480 : 137-169. Mani, M. 1989. A review of the pink mealy­ Berg, G.H. 1996. Analisis de riesgo por una bug - Maconellicoccus hirsutus (Green). via respecto a Maconellicoccus hirsutus Insect Sci. Applic. 10 : 157-167. (Green) (cochinilla rosada), a nivel glo­ Matile-Ferrero, D., and J. Etienne. 1996. bal. Informe teenico, OIRSA, El Salvador. Présence de la cochenille de l'hibiscus, 32 pp. Maconellicoccus hirsutus à Saint-Martin Dufour, B.P., and J. Léon. 1997. Informe de (Hemiptera : Pseudococcidae). Rev. Fr. mission de informacion sobre el control Entomol. 18 : 38. de la cochinilla rosada del hibisco (Ma­ conellicoccus hirsutus Green) en la ré­ gion del Caribe. IICA - El Salvador, 22 pp.

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Matile-Ferrero, D.f and J. Etienne. 1998. Para- Sagarra, L.A. 1999. Biology and behaviour coccus marginatus Williams & Granara of Anagyrus kamali Moursi [Homoptera : de Willink, nouvelle introduction en Pseudococcidae]. Ph.D. Thesis, McGill Guadeloupe et à Saint-Barthélémy (Hemi- University, Montréal, Canada. ptera : Pseudococcidae). Rev. Fr. Ento- Singh, M.P., and S.N. Ghosh. 1970. Studies mol. 20 : 148. on Maconellicoccus (Phenacoccus) hir- Me Comie, L. 1998. Incidence and treatment sutus Gr. causing "bunchytop" in M esta. of the hibiscus mealybug Maconellicoc­ Indian J. Sci. and Indust. 4 : 99-105. cus hirsutus(Gveen) inTrinidad. Proceed- Talhouk, A.S. 1993. Some insect species ing of the 1st seminar on the hibiscus injurious to crops in Middle East Coun- mealybug, April 1998, Trinidad. tries. J. Appl. Entomol. 116 : 105-111. Misra, C.S. 1919. "Tukra" disease of mulber- USDA. 1997. The pink hibiscus mealybug. ry. Proc. 3rd Entomol. Meet., Pusa. p. USDA Publication. Florida, USA. 610-618. Van Driesche, R.G., and T.S. Beliows. 1993. Panis, A. 1981. Note sur quelques insectes Steps in classical arthropod biological auxiliaires régulateurs des populations control. Thomas Say publications in de Pseudococcidae et Coccidae (Ho- entomology : proceedings. Maryland, moptera : Coccidea) des agrumes en USA. Provence orientale. Fruits 36 : 49-52. Williams, D.J. 1996. A brief account of the Pollard, G.V. 1998. Update on new pest in­ hibiscus mealybug Maconellicoccus hir- troductions. Circular Letter No. 3/98 - sutus (Hemiptera : Pseudococcidae), a FAO. pest of agriculture and horticulture, with Reddy, R.A. and L.K. Narayana. 1986. Biol- descriptions of two related species from ogy and control of grape mealybug. Indi- southern Asia. Bull. Entomol. Res. 86 : an Grape J. 2 : 30-39. 617-628.

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